A randomized phase II dose–response exercise trial among colon cancer survivors: Purpose, study design, methods, and recruitment results

Contemporary Clinical Trials

Volumn 47, Issue , 2016, Pages 366-375

  Brown, Justin C ^a   Troxel, Andrea B ^a   Ky, Bonnie ^a   Damjanov, Nevena ^a   Zemel, Babette S ^a,b   Rickels, Michael R ^a   Rhim, Andrew D ^c   Rustgi, Anil K ^a   Courneya, Kerry S ^d   Schmitz, Kathryn H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Energy balance; Lifestyle; Obesity; Physical activity; Quality of life; Survivorship

Indexed keywords

C PEPTIDE; GLYCOSYLATED HEMOGLOBIN; INSULIN; INTERCELLULAR ADHESION MOLECULE 1; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C;

ADULT; AEROBIC EXERCISE; AGED; ARTICLE; BLOOD SAMPLING; BODY COMPOSITION; CANCER SURVIVOR; CELL COUNTING; CIRCULATING TUMOR CELL; COLON CANCER; CONTROLLED STUDY; DIET RESTRICTION; DIETARY INTAKE; ELECTROCARDIOGRAM; EXERCISE INTENSITY; FEMALE; FUNCTIONAL STATUS; HEART RATE; HUMAN; INTRAABDOMINAL FAT; MAJOR CLINICAL STUDY; MALE; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PATIENT COMPLIANCE; PHASE 2 CLINICAL TRIAL; PHYSICAL ACTIVITY; PROGRAM FEASIBILITY; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL; SAFETY; SELF REPORT; TELEPHONE INTERVIEW; TREADMILL; TREADMILL EXERCISE; ADOLESCENT; CLINICAL PROTOCOL; CLINICAL TRIAL; COLONIC NEOPLASMS; EXERCISE; FEASIBILITY STUDY; KINESIOTHERAPY; METHODOLOGY; MIDDLE AGED; PATHOPHYSIOLOGY; PATIENT SELECTION; PHYSIOLOGY; PROCEDURES; SURVIVOR; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CLINICAL PROTOCOLS; COLONIC NEOPLASMS; EXERCISE; EXERCISE THERAPY; FEASIBILITY STUDIES; FEMALE; HUMANS; MALE; MIDDLE AGED; PATIENT SELECTION; QUALITY OF LIFE; RESEARCH DESIGN; SURVIVORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84982255245     PISSN: 15517144     EISSN: 15592030     Source Type: Journal    
DOI: 10.1016/j.cct.2016.03.001     Document Type: Article

References (85)

1. [1] Siegel, R., DeSantis, C., Jemal, A., Colorectal cancer statistics, 2014. CA Cancer J. Clin. 64 (2014), 104–117.
2. [2] DeSantis, C.E., Lin, C.C., Mariotto, A.B., Siegel, R.L., Stein, K.D., Kramer, J.L., et al. Cancer treatment and survivorship statistics, 2014. CA Cancer J. Clin., 2014.
3. [3] Clinical Outcomes of Surgical Therapy Study Group, A comparison of laparoscopically assisted and open colectomy for colon cancer. N. Engl. J. Med. 350 (2004), 2050–2059.
4. [4] Lacy, A.M., Garcia-Valdecasas, J.C., Delgado, S., Castells, A., Taura, P., Pique, J.M., et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359 (2002), 2224–2229.
5. [5] Meyerhardt, J.A., Mayer, R.J., Systemic therapy for colorectal cancer. N. Engl. J. Med. 352 (2005), 476–487.
6. [6] André, T., Boni, C., Mounedji-Boudiaf, L., Navarro, M., Tabernero, J., Hickish, T., et al. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med. 350 (2004), 2343–2351.
7. [7] Quasar Collaborative Group. Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomised study. Lancet 370 (2007), 2020–2029.
8. [8] Sargent, D.J., Wieand, H.S., Haller, D.G., Gray, R., Benedetti, J.K., Buyse, M., et al. Disease-free survival versus overall survival as a primary end point for adjuvant colon cancer studies: individual patient data from 20,898 patients on 18 randomized trials. J. Clin. Oncol. 23 (2005), 8664–8670.
9. [9] Meyerhardt, J.A., Heseltine, D., Niedzwiecki, D., Hollis, D., Saltz, L.B., Mayer, R.J., et al. Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J. Clin. Oncol. 24 (2006), 3535–3541.
10. [10] Meyerhardt, J.A., Giovannucci, E.L., Ogino, S., Kirkner, G.J., Chan, A.T., Willett, W., et al. Physical activity and male colorectal cancer survival. Arch. Intern. Med. 169 (2009), 2102–2108.
11. [11] Campbell, P.T., Patel, A.V., Newton, C.C., Jacobs, E.J., Gapstur, S.M., Associations of recreational physical activity and leisure time spent sitting with colorectal cancer survival. J. Clin. Oncol. 31 (2013), 876–885.
12. [12] Meyerhardt, J.A., Giovannucci, E.L., Holmes, M.D., Chan, A.T., Chan, J.A., Colditz, G.A., et al. Physical activity and survival after colorectal cancer diagnosis. J. Clin. Oncol. 24 (2006), 3527–3534.
13. [13] Kuiper, J.G., Phipps, A.I., Neuhouser, M.L., Chlebowski, R.T., Thomson, C.A., Irwin, M.L., et al. Recreational physical activity, body mass index, and survival in women with colorectal cancer. Cancer Causes Control, 2012.
14. [14] Je, Y., Jeon, J.Y., Giovannucci, E.L., Meyerhardt, J.A., Association between physical activity and mortality in colorectal cancer: a meta-analysis of prospective cohort studies. Int. J. Cancer 133 (2013), 1905–1913.
15. [15] Schmid, D., Leitzmann, M.F., Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann. Oncol. 25 (2014), 1293–1311.
16. [16] Des Guetz, G., Uzzan, B., Bouillet, T., Nicolas, P., Chouahnia, K., Zelek, L., et al. Impact of physical activity on cancer-specific and overall survival of patients with colorectal cancer. Gastroenterol. Res. Pract., 2013, 2013.
17. [17] Rock, C.L., Doyle, C., Demark-Wahnefried, W., Meyerhardt, J., Courneya, K.S., Schwartz, A.L., et al. Nutrition and physical activity guidelines for cancer survivors. CA Cancer J. Clin., 2012.
18. [18] Schmitz, K.H., Courneya, K.S., Matthews, C., Demark-Wahnefried, W., Galvao, D.A., Pinto, B.M., et al. American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med. Sci. Sports Exerc. 42 (2010), 1409–1426.
19. [19] National Comprehensive Cancer network, NCCN Clinical Practice Guidelines in Oncology: Survivorship. 2013, 2013.
20. [20] Paffenbarger, R.S. Jr., Blair, S.N., Lee, I.M., Hyde, R.T., Measurement of physical activity to assess health effects in free-living populations. Med. Sci. Sports Exerc. 25 (1993), 60–70.
21. [21] Pennsylvania Department of Health, Pennsylvania Cancer Registry (PCR). 2015.
22. [22] Rogerino, A., Grant, L.L., Wilcox, H. III, Schmitz, K.H., Geographic recruitment of breast cancer survivors into community-based exercise interventions. Med. Sci. Sports Exerc. 41 (2009), 1413–1420.
23. [23] Shephard, R.J., Readiness for Physical Activity. 1994, President's Council on Physical Fitness and Sports.
24. [24] Edge, S.B., Byrd, D.R., Compton, C.C., Fritz, A.G., Greene, F.L., Trotti, A., AJCC Cancer Staging Manual. 2010, Springer, New York.
25. [25] Von Korff, M., Wagner, E.H., Saunders, K., A chronic disease score from automated pharmacy data. J. Clin. Epidemiol. 45 (1992), 197–203.
26. [26] Craft, L.L., Guralnik, J.M., Ferrucci, L., Liu, K., Tian, L., Criqui, M.H., et al. Physical activity during daily life and circulating biomarker levels in patients with peripheral arterial disease. Am. J. Cardiol. 102 (2008), 1263–1268.
27. [27] Adamopoulos, S., Parissis, J., Kroupis, C., Georgiadis, M., Karatzas, D., Karavolias, G., et al. Physical training reduces peripheral markers of inflammation in patients with chronic heart failure. Eur. Heart J. 22 (2001), 791–797.
28. [28] Wallace, T.M., Levy, J.C., Matthews, D.R., Use and abuse of HOMA modeling. Diabetes Care 27 (2004), 1487–1495.
29. [29] Gleghorn, J.P., Pratt, E.D., Denning, D., Liu, H., Bander, N.H., Tagawa, S.T., et al. Capture of circulating tumor cells from whole blood of prostate cancer patients using geometrically enhanced differential immunocapture (GEDI) and a prostate-specific antibody. Lab Chip 10 (2010), 27–29.
30. [30] Zamboni, M., Turcato, E., Armellini, F., Kahn, H., Zivelonghi, A., Santana, H., et al. Sagittal abdominal diameter as a practical predictor of visceral fat. Int. J. Obes. 22 (1998), 655–660.
31. [31] Micklesfield, L.K., Goedecke, J.H., Punyanitya, M., Wilson, K.E., Kelly, T.L., Dual-energy X-ray performs as well as clinical computed tomography for the measurement of visceral fat. Obesity 20 (2012), 1109–1114.
32. [32] Bredella, M.A., Gill, C.M., Keating, L.K., Torriani, M., Anderson, E.J., Punyanitya, M., et al. Assessment of abdominal fat compartments using DXA in premenopausal women from anorexia nervosa to morbid obesity. Obesity 21 (2013), 2458–2464.
33. [33] ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories, ATS statement: guidelines for the six-minute walk test. Am. J. Respir. Crit. Care Med. 166 (2002), 111–117.
34. [34] Guyatt, G.H., Sullivan, M.J., Thompson, P.J., Fallen, E.L., Pugsley, S.O., Taylor, D.W., et al. The 6-minute walk: a new measure of exercise capacity in patients with chronic heart failure. Can. Med. Assoc. J. 132 (1985), 919–923.
35. [35] Ainsworth, B.E., Haskell, W.L., Whitt, M.C., Irwin, M.L., Swartz, A.M., Strath, S.J., et al. Compendium of physical activities: an update of activity codes and MET intensities. Med. Sci. Sports Exerc. 32 (2000), S498–S504.
36. [36] Bassett, D.R. Jr., Ainsworth, B.E., Swartz, A.M., Strath, S.J., O'Brien, W.L., King, G.A., Validity of four motion sensors in measuring moderate intensity physical activity. Med. Sci. Sports Exerc. 32 (2000), S471–S480.
37. [37] Troiano, R.P., Berrigan, D., Dodd, K.W., Masse, L.C., Tilert, T., McDowell, M., Physical activity in the United States measured by accelerometer. Med. Sci. Sports Exerc. 40 (2008), 181–188.
38. [38] Luhrmann, P.M., Herbert, B.M., Gaster, C., Neuhauser-Berthold, M., Validation of a self-administered 3-day estimated dietary record for use in the elderly. Eur. J. Nutr. 38 (1999), 235–240.
39. [39] Harrington, C.B., Hansen, J.A., Moskowitz, M., Todd, B.L., Feuerstein, M., It's not over when it's over: long-term symptoms in cancer survivors–a systematic review. Int. J. Psychiatry Med. 40 (2010), 163–181.
40. [40] Committee on Cancer Survivorship: Institute of Medicine and National Research Board, (eds.) From Cancer Patient to Cancer Survivor: Lost in Transition, 2006, The National Academic Press, Washington, DC.
41. [41] Ward, W.L., Hahn, E.A., Mo, F., Hernandez, L., Tulsky, D.S., Cella, D., Reliability and validity of the functional assessment of cancer therapy-colorectal (FACT-C) quality of life instrument. Qual. Life Res. 8 (1999), 181–195.
42. [42] Ware, J.E. Jr., Sherbourne, C.D., The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med. Care 30 (1992), 473–483.
43. [43] Cleeland, C.S., Ryan, K.M., Pain assessment: global use of the brief pain inventory. Ann. Acad. Med. Singap. 23 (1994), 129–138.
44. [44] Buysse, D.J., Reynolds, C.F. III, Monk, T.H., Berman, S.R., Kupfer, D.J., The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 28 (1989), 193–213.
45. [45] Haddock, M.G., Sloan, J.A., Bollinger, J.W., Soori, G., Steen, P.D., Martenson, J.A., et al. Patient assessment of bowel function during and after pelvic radiotherapy: results of a prospective phase III North Central Cancer Treatment Group clinical trial. J. Clin. Oncol. 25 (2007), 1255–1259.
46. [46] Mendoza, T.R., Wang, X.S., Cleeland, C.S., Morrissey, M., Johnson, B.A., Wendt, J.K., et al. The rapid assessment of fatigue severity in cancer patients: use of the brief fatigue inventory. Cancer 85 (1999), 1186–1196.
47. [47] Simard, S., Savard, J., Fear of cancer recurrence inventory: development and initial validation of a multidimensional measure of fear of cancer recurrence. Support. Care Cancer 17 (2009), 241–251.
48. [48] US Department of Health and Human Services, Common Terminology Criteria for Adverse Events (CTCAE) Version 4.0. 2009, National Institutes of Health, National Cancer Institute, 4.
49. [49] Brown, J.C., Troxel, A.B., Schmitz, K.H., Safety of weightlifting among women with or at risk for breast cancer-related lymphedema: musculoskeletal injuries and health care use in a weightlifting rehabilitation trial. Oncologist 17 (2012), 1120–1128.
50. [50] Warren, M., Schmitz, K.H., Safety of strength training in premenopausal women: musculoskeletal injuries from a two-year randomized trial. Am. J. Health Promot. 23 (2009), 309–314.
51. [51] Weinberg, R.S., Goal setting and performance in sport and exercise settings: a synthesis and critique. Med. Sci. Sports Exerc. 26 (1994), 469–477.
52. [52] Courneya, K.S., Booth, C.M., Gill, S., O'Brien, P., Vardy, J., Friedenreich, C.M., et al. The Colon health and life-long exercise change trial: a randomized trial of the National Cancer Institute of Canada clinical trials group. Curr. Oncol. 15 (2008), 279–285.
53. [53] Schmitz, K.H., Williams, N.I., Kontos, D., Domchek, S., Morales, K.H., Hwang, W., et al. Dose response effects of aerobic exercise on estrogen among women at high risk for breast cancer: a randomized controlled trial. Breast Cancer Res. Treat., 2015.
54. [54] Schmitz, K.H., Williams, N.I., Kontos, D., Kurzer, M., Schnall, M., Domchek, S., et al. Women in steady exercise research (WISER) sister: study design and methods. Contemp. Clin. Trials, 2015.
55. [55] Hamdy, O., Ledbury, S., Mullooly, C., Jarema, C., Porter, S., Ovalle, K., et al. Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome. Diabetes Care 26 (2003), 2119–2125.
56. [56] Leinonen, E., Hurt-Camejo, E., Wiklund, O., Hulten, L.M., Hiukka, A., Taskinen, M.R., Insulin resistance and adiposity correlate with acute-phase reaction and soluble cell adhesion molecules in type 2 diabetes. Atherosclerosis 166 (2003), 387–394.
57. [57] Tonjes, A., Scholz, M., Fasshauer, M., Kratzsch, J., Rassoul, F., Stumvoll, M., et al. Beneficial effects of a 4-week exercise program on plasma concentrations of adhesion molecules. Diabetes Care, 30, 2007, e1.
58. [58] Saetre, T., Enoksen, E., Lyberg, T., Stranden, E., Jorgensen, J.J., Sundhagen, J.O., et al. Supervised exercise training reduces plasma levels of the endothelial inflammatory markers E-selectin and ICAM-I in patients with peripheral arterial disease. Angiology 62 (2011), 301–305.
59. [59] Slentz, C.A., Aiken, L.B., Houmard, J.A., Bales, C.W., Johnson, J.L., Tanner, C.J., et al. Inactivity, exercise, and visceral fat. STRRIDE: a randomized, controlled study of exercise intensity and amount. J. Appl. Physiol. 99 (2005), 1613–1618.
60. [60] Slentz, C.A., Duscha, B.D., Johnson, J.L., Ketchum, K., Aiken, L.B., Samsa, G.P., et al. Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE—a randomized controlled study. Arch. Intern. Med. 164 (2004), 31–39.
61. [61] Slentz, C.A., Houmard, J.A., Kraus, W.E., Exercise, abdominal obesity, skeletal muscle, and metabolic risk: evidence for a dose response. Obesity 17 (2009), S27–S33.
62. [62] Houmard, J.A., Tanner, C.J., Slentz, C.A., Duscha, B.D., McCartney, J.S., Kraus, W.E., Effect of the volume and intensity of exercise training on insulin sensitivity. J. Appl. Physiol. (1985) 96 (2004), 101–106.
63. [63] Pinto, B.M., Papandonatos, G.D., Goldstein, M.G., Marcus, B.H., Farrell, N., Home-based physical activity intervention for colorectal cancer survivors. Psychooncology 22 (2013), 54–64.
64. [64] Ligibel, J.A., Meyerhardt, J., Pierce, J.P., Najita, J., Shockro, L., Campbell, N., et al. Impact of a telephone-based physical activity intervention upon exercise behaviors and fitness in cancer survivors enrolled in a cooperative group setting. Breast Cancer Res. Treat. 132 (2012), 205–213.
65. [65] Courneya, K.S., Vardy, J., Gill, S., Jonker, D., O'Brien, P., Friedenreich, C.M., et al. Update on the Colon Health and life-long exercise change trial: a phase III study of the impact of an exercise program on disease-free survival in colon cancer survivors. Curr. Color. Cancer Rep. 10 (2014), 321–328.
66. [66] van Waart, H., Stuiver, M.M., van Harten, W.H., Geleijn, E., Kieffer, J.M., Buffart, L.M., et al. Effect of low-intensity physical activity and moderate- to high-intensity physical exercise during adjuvant chemotherapy on physical fitness, fatigue, and chemotherapy completion rates: results of the PACES randomized clinical trial. J. Clin. Oncol. 33 (2015), 1918–1927.
67. [67] Meyerhardt, J., Exercise and Metformin in Colorectal and Breast Cancer Survivors 2013. 2013.
68. [68] Brown, J.C., Schmitz, K.H., The prescription or proscription of exercise in colorectal cancer care. Med. Sci. Sports Exerc. 46 (2014), 2202–2209.
69. [69] Beskow, L.M., Sandler, R.S., Weinberger, M., Research recruitment through US central cancer registries: balancing privacy and scientific issues. Am. J. Public Health, 96, 2006, 1920.
70. [70] Unger, J.M., Barlow, W.E., Martin, D.P., Ramsey, S.D., Leblanc, M., Etzioni, R., et al. Comparison of survival outcomes among cancer patients treated in and out of clinical trials. J. Natl. Cancer Inst., 106, 2014, dju002.
71. [71] Paschos, K.A., Canovas, D., Bird, N.C., The role of cell adhesion molecules in the progression of colorectal cancer and the development of liver metastasis. Cell. Signal. 21 (2009), 665–674.
72. [72] Howard, K., Lo, K.K., Ao, L., Gamboni, F., Edil, B.H., Schulick, R., et al. Intercellular adhesion molecule-1 mediates murine colon adenocarcinoma invasion. J. Surg. Res. 187 (2014), 19–23.
73. [73] Schlesinger, M., Bendas, G., Vascular cell adhesion molecule-1 (VCAM-1)—an increasing insight into its role in tumorigenicity and metastasis. Int. J. Cancer 136 (2015), 2504–2514.
74. [74] Giavazzi, R., Chirivi, R.G., Garofalo, A., Rambaldi, A., Hemingway, I., Pigott, R., et al. Soluble intercellular adhesion molecule 1 is released by human melanoma cells and is associated with tumor growth in nude mice. Cancer Res. 52 (1992), 2628–2630.
75. [75] Nakashio, T., Narita, T., Sato, M., Akiyama, S., Kasai, Y., Fujiwara, M., et al. The association of metastasis with the expression of adhesion molecules in cell lines derived from human gastric cancer. Anticancer Res. 17 (1997), 293–299.
76. [76] Aoi, W., Naito, Y., Takagi, T., Tanimura, Y., Takanami, Y., Kawai, Y., et al. A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise. Gut 62 (2013), 882–889.
77. [77] Rickles, A.S., Iannuzzi, J.C., Mironov, O., Deeb, A., Sharma, A., Fleming, F.J., et al. Visceral obesity and colorectal cancer: are we missing the boat with BMI?. J. Gastrointest. Surg. 17 (2013), 133–143.
78. [78] Moon, H.G., Ju, Y.T., Jeong, C.Y., Jung, E.J., Lee, Y.J., Hong, S.C., et al. Visceral obesity may affect oncologic outcome in patients with colorectal cancer. Ann. Surg. Oncol. 15 (2008), 1918–1922.
79. [79] Guiu, B., Petit, J.M., Bonnetain, F., Ladoire, S., Guiu, S., Cercueil, J., et al. Visceral fat area is an independent predictive biomarker of outcome after first-line bevacizumab-based treatment in metastatic colorectal cancer. Gut 59 (2010), 341–347.
80. [80] Ballian, N., Lubner, M.G., Munoz, A., Harms, B.A., Heise, C.P., Foley, E.F., et al. Visceral obesity is associated with outcomes of total mesorectal excision for rectal adenocarcinoma. J. Surg. Oncol. 105 (2012), 365–370.
81. [81] Haydon, A.M., Macinnis, R.J., English, D.R., Giles, G.G., Effect of physical activity and body size on survival after diagnosis with colorectal cancer. Gut 55 (2006), 62–67.
82. [82] Prizment, A.E., Flood, A., Anderson, K.E., Folsom, A.R., Survival of women with colon cancer in relation to precancer anthropometric characteristics: the Iowa Women's Health Study. Cancer Epidemiol. Biomarkers Prev. 19 (2010), 2229–2237.
83. [83] Jiang, B., Zhang, X., Du, L., Wang, Y., Liu, D., Han, C., et al. Possible roles of insulin, IGF-1 and IGFBPs in initiation and progression of colorectal cancer. World J. Gastroenterol., 20, 2014, 1608.
84. [84] Sandhu, M.S., Dunger, D.B., Giovannucci, E.L., Insulin, insulin-like growth factor-I (IGF-I), IGF binding proteins, their biologic interactions, and colorectal cancer. J. Natl. Cancer Inst. 94 (2002), 972–980.
85. [85] Giovannucci, E., Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J. Nutr. 131 (2001), 3109S–3120S.